Roles of YehZ, a Putative Osmoprotectant Transporter, in Tempering Growth of Salmonella enterica serovar Typhimurium

Kim, Seul I; Ryu, Sangryeol; Yoon, Hyun Jin

doi:10.4014/jmb.1308.08006

Cited by 17 publications

(16 citation statements)

References 48 publications

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“…However, the function of YehZYXW in vivo remains unclear. The sensitivity of an S. enterica ΔyehZ strain to hyperosmotic shock is similar to that of the wild type, though the strain is reported to grow faster in medium of standard osmolality and to replicate more efficiently than the wild type in macrophages (20). In E. coli, YehZ is reported to interact with glycine betaine with very low affinity (K d [equilibrium dissociation constant] Ϸ 2 mM) and to participate in its uptake, though the yehZ gene confers no protection against hyperosmotic shock in the presence of glycine betaine (19).…”

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“…The PBP component of the operon (gene locus bab1_0226) is most closely related to Escherichia coli and Salmonella enterica YehZ, which has been described as a component of a putative compatible solute osmoprotectant transport system, YehZYXW (17)(18)(19)(20). The Yeh system is related in primary structure to the glycine betaine OsmU/ ProU uptake systems of S. enterica and E. coli and the OpuB/OpuC choline transporter of Bacillus subtilis (17,(20)(21)(22)(23). However, the function of YehZYXW in vivo remains unclear.…”

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confidence: 99%

“…In E. coli, YehZ is reported to interact with glycine betaine with very low affinity (K d [equilibrium dissociation constant] Ϸ 2 mM) and to participate in its uptake, though the yehZ gene confers no protection against hyperosmotic shock in the presence of glycine betaine (19). In both E. coli and S. enterica, transcription of YehZ is under the control of the general stress factor, s , and is activated by stress conditions, including nutrient limitation, acidic pH, and hyperosmotic shock (17,20). Analogous to s activation of YehZ expression in E. coli, transcription of B. abortus bab1_0226 is activated by the GSR sigma factor, E1 ( EcfG ) (24,25).…”

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Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria

et al. 2017

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Brucella abortus E1 is an EcfG family sigma factor that regulates the transcription of dozens of genes in response to diverse stress conditions and is required for maintenance of chronic infection in a mouse model. A putative ATPbinding cassette transporter operon, bab1_0223-bab1_0226, is among the most highly activated gene sets in the E1 regulon. The proteins encoded by the operon resemble quaternary ammonium-compatible solute importers but are most similar in sequence to the broadly conserved YehZYXW system, which remains largely uncharacterized. Transcription of yehZYXW is activated by the general stress sigma factor S in Enterobacteriaceae, which suggests a functional role for this transport system in bacterial stress response across the classes Alphaproteobacteria and Gammaproteobacteria. We present evidence that B. abortus YehZYXW does not function as an importer of known compatible solutes under physiological conditions and does not contribute to the virulence defect of a E1 -null strain. The sole in vitro phenotype associated with genetic disruption of this putative transport system is reduced growth in the presence of high Li ϩ ion concentrations. A crystal structure of B. abortus YehZ revealed a class II periplasmic binding protein fold with significant structural homology to Archaeoglobus fulgidus ProX, which binds glycine betaine. However, the structure of the YehZ ligand-binding pocket is incompatible with high-affinity binding to glycine betaine. This is consistent with weak measured binding of YehZ to glycine betaine and related compatible solutes. We conclude that YehZYXW is a conserved, stress-regulated transport system that is phylogenetically and functionally distinct from quaternary ammonium-compatible solute importers.IMPORTANCE Brucella abortus E1 regulates transcription in response to stressors encountered in its mammalian host and is necessary for maintenance of chronic infection in a mouse model. The functions of the majority of genes regulated by E1 remain undefined. We present a functional/structural analysis of a conserved putative membrane transport system (YehZYXW) whose expression is strongly activated by E1 . Though annotated as a quaternary ammonium osmolyte uptake system, experimental physiological studies and measured ligand-binding properties of the periplasmic binding protein (PBP), YehZ, are inconsistent with this function. A crystal structure of B. abortus YehZ provides molecular insight into differences between bona fide quaternary ammonium osmolyte importers and YehZ-related proteins, which form a distinct phylogenetic and functional group of PBPs.

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Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria

et al. 2017

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“…syringae B728a [42], because it is 97% identical to the included OpuCC from Pseudomonas syringae pv. syringae DC3000; YehZ from Salmonella typhimurium [46], because it is 88% identical to EcYehZ and its substrate is unknown; and ProX from Agrobacterium tumefaciens, because no data apart from crystal structures (PDB ID 4NE4 and 4ND9) are available. substrate is coordinated via three tryptophan residues (e.g., OpuAC from L. lactis [37] and ProX from Escherichia coli [38]) or four tyrosines (e.g., ProX from Archaeoglobus fulgidus [33]).…”

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confidence: 99%

Crystal Structure of the Substrate-Binding Domain from Listeria monocytogenes Bile-Resistance Determinant BilE

2016

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BilE has been reported as a bile resistance determinant that plays an important role in colonization of the gastrointestinal tract by Listeria monocytogenes, the causative agent of listeriosis. The mechanism(s) by which BilE mediates bile resistance are unknown. BilE shares significant sequence similarity with ATP-binding cassette (ABC) importers that contribute to virulence and stress responses by importing quaternary ammonium compounds that act as compatible solutes. Assays using related compounds have failed to demonstrate transport mediated by BilE. The putative substrate-binding domain (SBD) of BilE was expressed in isolation and the crystal structure solved at 1.5 Å. Although the overall fold is characteristic of SBDs, the binding site varies considerably relative to the well-characterized homologs ProX from Archaeoglobus fulgidus and OpuBC and OpuCC from Bacillus subtilis. This suggests that BilE may bind an as-yet unknown ligand. Elucidation of the natural substrate of BilE could reveal a novel bile resistance mechanism.

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“…Herein, we illustrated that the yehZ gene coding for a putative ABC superfamily transport protein was induced in the stressed strain. Recently, the role of YehZ was characterized as an osmoprotectant transporter in S. Typhimurium, restraining trehalose production [40]. The acrA gene coding for an acridine efflux pump was also induced in the stressed S. Typhimurium strain.…”

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confidence: 99%

Molecular analysis of the adaptive response in Salmonella Typhimurium after starvation in salty conditions

Elabed

Merghni

Hamza

et al. 2016

J Infect Dev Ctries

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Introduction: The pathogenic bacterium Salmonella enterica serovar Typhimurium elicits a variety of genetic programs to adapt to stress conditions encountered within hostile environments such as host phagocytes and preserved food. Methodology: In this work, differential display (DD) methodology was used to investigate the effect of one month starvation in a salty microcosm (0.5 M NaCl) on transcript profiling in a Salmonella Typhimurium LT2 strain. cDNA fragments resulting from differentially expressed mRNA were eluted from the gel, re-amplified, cloned, and then sequenced. Results: A total of 21 differentially expressed bands were detected by DD reverse transcription-polymerase chain reaction (RT-PCR). However, only 12 of them were successfully identified as upregulated genes in stressed cells. Based on the sequencing data and BLAST analysis, these genes were sopA, ssaD, yhhK, gmK, cspC, uspA, ompR, phoP, stcC, fimA, acrA,and yehZ. As a confirmation of the differential expression, RT-PCR was carried out using a set of specific primers. Remarkably, the expression levels of these genes were significantly increased in starved bacteria compared to standard laboratory conditions. Conclusions: Our results indicate that the starvation of Salmonella Typhimurium over one month in a salty microcosm changes the expression of stress proteins, response regulator in a two-component system, outer membrane proteins, effector proteins translocated by Salmonella pathogenicity island SPI1 and SPI2 type III secretion systems (TTSS), several metabolic enzymes, efflux pumps, and transport proteins. This suggests that the expression of the identified genes is important for the response of this pathogen to starvation in salt.

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Roles of YehZ, a Putative Osmoprotectant Transporter, in Tempering Growth of Salmonella enterica serovar Typhimurium

Cited by 17 publications

References 48 publications

Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria

Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria

Crystal Structure of the Substrate-Binding Domain from Listeria monocytogenes Bile-Resistance Determinant BilE

Molecular analysis of the adaptive response in Salmonella Typhimurium after starvation in salty conditions

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